Temporal proteomic profiling reveals insight into critical developmental processes and temperature-influenced physiological response differences in a bivalve mollusc

Abstract Background Protein expression patterns underlie physiological processes and phenotypic differences including those occurring during early development. The Pacific oyster (Crassostrea gigas) undergoes a major phenotypic change in early development from free-swimming larval form to sessile be...

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Main Authors: Trigg, Shelly A., Mitchell, Kaitlyn R., Thompson, Rhonda Elliott, Benoit Eudeline, Vadopalas, Brent, Timmins-Schiffman, Emma B., Roberts, Steven B.
Format: Article in Journal/Newspaper
Language:unknown
Published: figshare 2020
Subjects:
Online Access:https://dx.doi.org/10.6084/m9.figshare.c.5180070
https://springernature.figshare.com/collections/Temporal_proteomic_profiling_reveals_insight_into_critical_developmental_processes_and_temperature-influenced_physiological_response_differences_in_a_bivalve_mollusc/5180070
id ftdatacite:10.6084/m9.figshare.c.5180070
record_format openpolar
spelling ftdatacite:10.6084/m9.figshare.c.5180070 2023-05-15T15:59:03+02:00 Temporal proteomic profiling reveals insight into critical developmental processes and temperature-influenced physiological response differences in a bivalve mollusc Trigg, Shelly A. Mitchell, Kaitlyn R. Thompson, Rhonda Elliott Benoit Eudeline Vadopalas, Brent Timmins-Schiffman, Emma B. Roberts, Steven B. 2020 https://dx.doi.org/10.6084/m9.figshare.c.5180070 https://springernature.figshare.com/collections/Temporal_proteomic_profiling_reveals_insight_into_critical_developmental_processes_and_temperature-influenced_physiological_response_differences_in_a_bivalve_mollusc/5180070 unknown figshare https://dx.doi.org/10.1186/s12864-020-07127-3 Creative Commons Attribution 4.0 International https://creativecommons.org/licenses/by/4.0/legalcode cc-by-4.0 CC-BY Ecology FOS Biological sciences Collection article 2020 ftdatacite https://doi.org/10.6084/m9.figshare.c.5180070 https://doi.org/10.1186/s12864-020-07127-3 2021-11-05T12:55:41Z Abstract Background Protein expression patterns underlie physiological processes and phenotypic differences including those occurring during early development. The Pacific oyster (Crassostrea gigas) undergoes a major phenotypic change in early development from free-swimming larval form to sessile benthic dweller while proliferating in environments with broad temperature ranges. Despite the economic and ecological importance of the species, physiological processes occurring throughout metamorphosis and the impact of temperature on these processes have not yet been mapped out. Results Towards this, we comprehensively characterized protein abundance patterns for 7978 proteins throughout metamorphosis in the Pacific oyster at different temperature regimes. We used a multi-statistical approach including principal component analysis, ANOVA-simultaneous component analysis, and hierarchical clustering coupled with functional enrichment analysis to characterize these data. We identified distinct sets of proteins with time-dependent abundances generally not affected by temperature. Over 12 days, adhesion and calcification related proteins acutely decreased, organogenesis and extracellular matrix related proteins gradually decreased, proteins related to signaling showed sinusoidal abundance patterns, and proteins related to metabolic and growth processes gradually increased. Contrastingly, different sets of proteins showed temperature-dependent abundance patterns with proteins related to immune response showing lower abundance and catabolic pro-growth processes showing higher abundance in animals reared at 29 °C relative to 23 °C. Conclusion Although time was a stronger driver than temperature of metamorphic proteome changes, temperature-induced proteome differences led to pro-growth physiology corresponding to larger oyster size at 29 °C, and to altered specific metamorphic processes and possible pathogen presence at 23 °C. These findings offer high resolution insight into why oysters may experience high mortality rates during this life transition in both field and culture settings. The proteome resource generated by this study provides data-driven guidance for future work on developmental changes in molluscs. Furthermore, the analytical approach taken here provides a foundation for effective shotgun proteomic analyses across a variety of taxa. Article in Journal/Newspaper Crassostrea gigas Pacific oyster DataCite Metadata Store (German National Library of Science and Technology) Pacific
institution Open Polar
collection DataCite Metadata Store (German National Library of Science and Technology)
op_collection_id ftdatacite
language unknown
topic Ecology
FOS Biological sciences
spellingShingle Ecology
FOS Biological sciences
Trigg, Shelly A.
Mitchell, Kaitlyn R.
Thompson, Rhonda Elliott
Benoit Eudeline
Vadopalas, Brent
Timmins-Schiffman, Emma B.
Roberts, Steven B.
Temporal proteomic profiling reveals insight into critical developmental processes and temperature-influenced physiological response differences in a bivalve mollusc
topic_facet Ecology
FOS Biological sciences
description Abstract Background Protein expression patterns underlie physiological processes and phenotypic differences including those occurring during early development. The Pacific oyster (Crassostrea gigas) undergoes a major phenotypic change in early development from free-swimming larval form to sessile benthic dweller while proliferating in environments with broad temperature ranges. Despite the economic and ecological importance of the species, physiological processes occurring throughout metamorphosis and the impact of temperature on these processes have not yet been mapped out. Results Towards this, we comprehensively characterized protein abundance patterns for 7978 proteins throughout metamorphosis in the Pacific oyster at different temperature regimes. We used a multi-statistical approach including principal component analysis, ANOVA-simultaneous component analysis, and hierarchical clustering coupled with functional enrichment analysis to characterize these data. We identified distinct sets of proteins with time-dependent abundances generally not affected by temperature. Over 12 days, adhesion and calcification related proteins acutely decreased, organogenesis and extracellular matrix related proteins gradually decreased, proteins related to signaling showed sinusoidal abundance patterns, and proteins related to metabolic and growth processes gradually increased. Contrastingly, different sets of proteins showed temperature-dependent abundance patterns with proteins related to immune response showing lower abundance and catabolic pro-growth processes showing higher abundance in animals reared at 29 °C relative to 23 °C. Conclusion Although time was a stronger driver than temperature of metamorphic proteome changes, temperature-induced proteome differences led to pro-growth physiology corresponding to larger oyster size at 29 °C, and to altered specific metamorphic processes and possible pathogen presence at 23 °C. These findings offer high resolution insight into why oysters may experience high mortality rates during this life transition in both field and culture settings. The proteome resource generated by this study provides data-driven guidance for future work on developmental changes in molluscs. Furthermore, the analytical approach taken here provides a foundation for effective shotgun proteomic analyses across a variety of taxa.
format Article in Journal/Newspaper
author Trigg, Shelly A.
Mitchell, Kaitlyn R.
Thompson, Rhonda Elliott
Benoit Eudeline
Vadopalas, Brent
Timmins-Schiffman, Emma B.
Roberts, Steven B.
author_facet Trigg, Shelly A.
Mitchell, Kaitlyn R.
Thompson, Rhonda Elliott
Benoit Eudeline
Vadopalas, Brent
Timmins-Schiffman, Emma B.
Roberts, Steven B.
author_sort Trigg, Shelly A.
title Temporal proteomic profiling reveals insight into critical developmental processes and temperature-influenced physiological response differences in a bivalve mollusc
title_short Temporal proteomic profiling reveals insight into critical developmental processes and temperature-influenced physiological response differences in a bivalve mollusc
title_full Temporal proteomic profiling reveals insight into critical developmental processes and temperature-influenced physiological response differences in a bivalve mollusc
title_fullStr Temporal proteomic profiling reveals insight into critical developmental processes and temperature-influenced physiological response differences in a bivalve mollusc
title_full_unstemmed Temporal proteomic profiling reveals insight into critical developmental processes and temperature-influenced physiological response differences in a bivalve mollusc
title_sort temporal proteomic profiling reveals insight into critical developmental processes and temperature-influenced physiological response differences in a bivalve mollusc
publisher figshare
publishDate 2020
url https://dx.doi.org/10.6084/m9.figshare.c.5180070
https://springernature.figshare.com/collections/Temporal_proteomic_profiling_reveals_insight_into_critical_developmental_processes_and_temperature-influenced_physiological_response_differences_in_a_bivalve_mollusc/5180070
geographic Pacific
geographic_facet Pacific
genre Crassostrea gigas
Pacific oyster
genre_facet Crassostrea gigas
Pacific oyster
op_relation https://dx.doi.org/10.1186/s12864-020-07127-3
op_rights Creative Commons Attribution 4.0 International
https://creativecommons.org/licenses/by/4.0/legalcode
cc-by-4.0
op_rightsnorm CC-BY
op_doi https://doi.org/10.6084/m9.figshare.c.5180070
https://doi.org/10.1186/s12864-020-07127-3
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